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Journal Pre-Proof Journal Pre-proof Prodiamesa olivacea: de novo biomarker genes in a potential sentinel organism for ecotoxicity studies in natural scenarios<!–<ForCover>Llorente L, Herrero O,´ Aquilino M, PlanelloR,´ Prodiamesa olivacea: de novo biomarker genes in a potential sentinel organism for ecotoxicity studies in natural scenarios, Aquatic Toxicology, doi: 10.1016/j.aquatox.2020.105593</ForCover>–> Lola Llorente (Investigation) (Data curation) (Writing - original draft) (Formal analysis), Oscar´ Herrero (Resources) (Methodology) (Writing - review and editing), Monica´ Aquilino (Visualization) (Writing - review and editing), Rosario Planello´ (Resources) (Supervision) (Funding acquisition) (Writing - review and editing) PII: S0166-445X(20)30343-X DOI: https://doi.org/10.1016/j.aquatox.2020.105593 Reference: AQTOX 105593 To appear in: Aquatic Toxicology Received Date: 3 March 2020 Revised Date: 30 July 2020 Accepted Date: 3 August 2020 Please cite this article as: { doi: https://doi.org/ This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier. Prodiamesa olivacea: de novo biomarker genes in a potential sentinel organism for ecotoxicity studies in natural scenarios. Lola Llorente1, Óscar Herrero1, Mónica Aquilino1, Rosario Planelló1* 1 Biology and Environmental Toxicology Group, Faculty of Sciences, Universidad Nacional de Educación a Distancia (UNED), Paseo de la Senda del Rey 9, 28040 Madrid, Spain. Email or corresponding author: [email protected] Highlights P. olivacea and C. riparius were used to assess the toxic effects of BBP, BPA and BP3 New genes for detoxification and oxidative stress were characterized in P. olivacea Transcript levels of the studied genes showed alterations after xenobiotic exposure Genes related to the oxidative stress response presented species-dependent responses P. olivacea could be a suitable sentinel organism for aquatic toxicity tests of EDCs Journal Pre-proof 1 Abstract Along with traditional ecotoxicological approaches in model organisms, toxicological studies in non-model organisms are being taken into consideration in order to complement them and contribute to more robust approaches. This allows us to figure out the complexity of the exposures involved in natural ecosystems. In this context, in the present research we have used the model species Chironomus riparius (Chironomidae, Diptera) and the non-model species Prodiamesa olivacea (Chironomidae, Diptera) to assess the aquatic toxic effects of acute 4-h and 24-h exposures to 1 µgL-1 of three common environmental pollutants: butyl benzyl phthalate (BBP), bisphenol A (BPA), and benzophenone 3 (BP3). Individuals of both species were collected from a contaminated river (Sar) in Galicia (Spain). Regarding Chironomus, there are four OECD standardized tests for the evaluation of water and sediment toxicity, in which different species in this genus can be used to assess classical toxicity parameters such as survival, immobilization, reproduction, and development. In contrast, Prodiamesa is rarely used in toxicity studies, even though it is an interesting toxicological species because it shares habitats with Chironomus but requires less extreme conditions (e.g., contamination) and higher oxygen levels. These different requirements are particularly interesting in assessing the different responses of both species to pollutant exposure. Quantitative real-time PCR was used to evaluate the transcriptional changes caused by xenobiotics in different genes of interest. Since information about P. olivacea in genomic databases is scarce, its transcriptome was obtained using de novo RNAseq. Genes involved in biotransformation pathways and the oxidative stress response (MnSODJournal, CAT, PHGPx, Cyp4g15, Cyp6a14 -Pre-prooflike and Cyp6a2-like) were de novo identified in this species. Our results show differential toxic responses depending on the species and the xenobiotic, being P. olivacea the dipteran that showed the most severe effects in most of the studied biomarker genes. 2 This work represents a multi-species approach that allows us to deepen in the toxicity of BBP, BPA, and BP3 at the molecular level. Besides, it provides an assessment of the tolerance/sensitivity of natural populations of model and non-model insect species chronically exposed to complex mixtures of pollutants in natural scenarios. These findings may have important implications for understanding the adverse biological effects of xenobiotics on P. olivacea, providing new sensitive biomarkers of exposure to BBP, BPA, and BP3. It also highlights the suitability of Prodiamesa for ecotoxicological risk assessment, especially in aquatic ecosystems. Keywords Transcriptional biomarker, detoxification, oxidative stress, emergent pollutants, sentinel organism, endocrine disruptor Journal Pre-proof 3 Introduction Water pollution can be caused in many ways, including direct sources such as effluent outfalls (from factories, waste treatment plants, etc.), and indirect sources in which contaminants enter the aquatic systems from soils or groundwater systems and the atmosphere via rainwater. Substances such as fertilizers, pesticides, herbicides, and a wide variety of toxic chemicals enter the dynamics of the ecosystems, disrupt the physical or biological components of the aquatic environments, and can lead to shifts in the viability of their populations. Among the polluting substances, those that are most persistent in the environment often give rise to a particular concern, since the effects resulting from their exposure can be prolonged over time. In this regard, butyl benzyl phthalate (BBP), bisphenol A (BPA), and benzophenone 3 (BP3) are ubiquitous contaminants whose presence in the environment is expected for decades. The primary use of BBP is as a softener (plasticizer) in PVC products, but it is also used in sealants, adhesives, paints, inks and lacquers, car care products, cosmetics, food conveyor belts, or vinyl gloves (CPSC, 2010; EC, 2007). Based on its widespread use worldwide, it is considered a global pollutant. According to Annex I of Directive 67/548/EEC, this substance is classified as toxic to reproduction in humans, capable of damaging the unborn child and with a possible risk of causing infertility. It is further classified as very toxic to aquatic organisms, and susceptible to cause long-term adverse effects in aquatic environments (EC, 2007; EFSA, 2019). Alterations caused by BBP in the ecdysone hormone pathway, the cellular response to stress, the energy metabolism, and several detoxification mechanisms have been described in Chironomus riparius larvae (Herrero et al., 2015; Planelló et al., 2011). BPA is Journalalso considered a ubiquitous pollutant. Pre-proof It is mainly used in the manufacture of polycarbonate plastics, epoxy resins, or thermal papers, and its release to the environment can occur from long-life materials used in flooring, furniture, toys, construction, curtains, foot-wear, leather products, paper and cardboard products, electronic equipment (ECHA, 2020a). BPA is classified as toxic for reproduction, and 4 also as a skin-sensitizing product and an endocrine-disrupting chemical. Based on its toxic properties, in recent years, its use in toys, thermal paper, and materials in contact with food has been restricted (ECHA, 2020b). It is a representative endocrine disruptor in both vertebrate and invertebrate species, including chironomids (Lee and Choi, 2007; Planelló et al., 2008). BP3 is one of the most frequently used UV filters, and it is also included in a variety of products to protect them from light damage. Due to the extensive use of sunscreens, it has been detected in natural water, sediments, and even in tap water (Kim and Choi, 2014; Ramos et al., 2015). Although the compound displays a low acute toxicity profile (EC, 2008), it is currently under assessment due to its endocrine-disrupting properties (ECHA, 2020c). In recent years, some studies tried to elucidate the molecular effects of BP3 in C. riparius, and alterations on relevant genes (related to the endocrine system, detoxification mechanisms, and the stress response), enzyme activities (immune system, oxidative stress), and the emergence and development rates have been described (Campos et al., 2019; Martín-Folgar et al., 2018; Muñiz-González and Martínez-Guitarte, 2020). The selection of appropriate protocols for the study of contaminants in invertebrates is one of the priority objectives for the evaluation of their environmental impact (OECD, 2006). Species selection should be based on the ecological relevance of the group of invertebrates to which they belong, and the existence of standardized tests. Macroinvertebrates are useful organisms in water quality monitoring, and their presence or absence are indicators of the degree of contamination (Gresens et al., 2009). In this group of animals, the use of chironomids as bioindicators have significantlyJournal increased in the last decades (ArimoroPre-proof et al., 2018; Ospina‐Pérez et al., 2019; Rosenberg,
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